PLoS BIOLOGY
Active Spatial Perception in the Vibrissa
Scanning Sensorimotor System
Samar B. Mehta1, Diane Whitmer2,3, Rodolfo Figueroa4, Ben A. Williams5, David Kleinfeld1,2,4,6
1 Neurosciences Graduate Program, University of California at San Diego, La Jolla, California, United States of America, 2 Computational Neurobiology Graduate Program,
University of California at San Diego, La Jolla, California, United States of America, 3 Division of Biological Sciences, University of California at San Diego, La Jolla, California,
United States of America, 4 Department of Physics, University of California at San Diego, La Jolla, California, United States of America, 5 Department of Psychology, University
of California at San Diego, La Jolla, California, United States of America, 6 Center for Theoretical Biological Physics, University of California at San Diego, La Jolla, California,
United States of America
Haptic perception is an active process that provides an awareness of objects that are encountered as an organism
scans its environment. In contrast to the sensation of touch produced by contact with an object, the perception of
object location arises from the interpretation of tactile signals in the context of the changing configuration of the body.
A discrete sensory representation and a low number of degrees of freedom in the motor plant make the ethologically
prominent rat vibrissa system an ideal model for the study of the neuronal computations that underlie this perception.
We found that rats with only a single vibrissa can combine touch and movement to distinguish the location of objects
that vary in angle along the sweep of vibrissa motion. The patterns of this motion and of the corresponding behavioral
responses show that rats can scan potential locations and decide which location contains a stimulus within 150 ms. This
interval is consistent with just one to two whisk cycles and provides constraints on the underlying perceptual
computation. Our data argue against strategies that do not require the integration of sensory and motor modalities.
The ability to judge angular position with a single vibrissa thus connects previously described, motion-sensitive
neurophysiological signals to perception in the behaving animal.
Citation: Mehta SB, Whitmer D, Figueroa R, Williams BA, Kleinfeld D (2007) Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol 5(2): e15. doi:10.
1371/journal.pbio.0050015
few experiments, to our knowledge, have explicitly characterized the spatial information available from the vibrissae.
Early work indicated that rats use this system for the
detection of surfaces during navigation [14], and more recent
studies have shown that the vibrissae provide information
about object distance [15,16], shape [17], and orientation
[18,19]. Few of these behaviors inherently engaged the
sensorimotor nature of the system, and rats are known to
perform some tasks, such as vibration [20] and bilateral
distance [21] discrimination, with only passive vibrissa
contacts. The system as a whole, in contrast, is fundamentally
active. Of the many mammalian species with vibrissae [22],
rats and related rodent species have specifically evolved the
ability to sweep their vibrissae for dynamic exploration of the
environment [23]. This ability leads us to question whether
touch and motion are used in concert, in the spirit of Gibson,
to form an ‘‘active perceptual system.’’
Neurophysiologically, the sensory and motor processes are
tightly interwoven. A nested series of loops, at levels from
brainstem to cortex, connects the vibrissa sensory stream to a
hierarchical motor drive that ordinarily produces a rhythmic
rostrocaudal movement known as exploratory whisking [24].
Sensory inputs feed back onto motor areas at all levels and
Introduction
‘‘Neurophysiologists. . .have been reluctant to face up to
[changes in anatomy from moment to moment] in explaining
perception, for they know more about the anatomy of the
eyes, ears, and skin than they do about the physiology of
looking, listening, and touching’’ – J. J. Gibson [1].
The noted psychologist J. J. Gibson argued forty years ago
[1] that the sensations produced by feed-forward transformation of inputs from neuronal exteroreceptors are
distinct from the dynamic perception of the environment
derived from the ‘‘neural loops of an active perceptual
system’’. Gibson’s thesis was that the perception of the
location of a contacted object, for example, is fundamentally
different from the sense impressions that arise from skin
mechanotransduction. Perception requires an integration of
information across sensory and motor modalities that is not
necessarily derived from successive transformations of the
touch data alone. Studies in systems from posture control
[2,3] to eye movement [4] have elucidated principles of such
‘‘neural loops’’ when used in motor systems with explicit
sensory feedback. The work described here addresses the
complementary case of positional context in a sensory system
with explicit motor drive [5,6].
The rat vibrissa system, with its tactile hairs and their
associated neuronal architecture, provides our prototype for
this sensorimotor model. For nearly a century, researchers
have compiled behavioral evidence that the vibrissae are both
sensors and effectors in a complex sensory system that is able
to identify and locate objects [7]. Although recent insights
into the mechanical properties of the vibrissae [8,9] may
explain the processing of qualities such as texture [10–13],
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Academic Editor: Markus Meister, Harvard University, United States of America
Received July 25, 2006; Accepted November 13, 2006; Published January 16, 2007
Copyright: Ó 2007 Mehta et al. This is an open-access article distributed under the
terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author
and source are credited.
Abbreviations: K-S, Kolmogorov-Smirnov
* To whom correspondence should be addressed. E-mail: dk@physics.ucsd.edu
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Author Summary
Rats explore the world with their whiskers (vibrissae). Although the
sensations of touch that an animal experiences while exploring an
object either in front of its head or to its side can be similar, the two
sensations tell the animal different things about its nearby environment. The translation from passive touch to knowledge of an
object’s location requires that the nervous system keep track of the
location of the animal’s body as it moves. We studied this process by
restricting a rat’s whisking information to that provided by a single
actively moving vibrissa. We found that even with such limited
information, rats can search for, locate, and differentiate objects
near their heads with astonishing speed. Their behavior during this
search reflects the computations performed by their nervous
systems to locate objects based on touch, and this behavior
demonstrates that rats keeps track of their vibrissa motion with a
resolution of less than 0.1 s. Understanding how these computations
are performed will bring us closer to understanding how the brain
integrates the sense of touch with its sense of self.
can alter motor output at even the lowest-order brainstem
loops [25]. The information flow is bidirectional, however,
and electrophysiological recordings have found neurons,
again at levels from the brainstem to cortex, that encode
the changing position of the vibrissae even in the absence of
contact with an external object [26–29]. These cells complement somatosensory neurons that encode the qualities of
contact and could provide the brain with an internal
reference as self-generated motion modulates the external
location that corresponds to contact.
The existence of position-sensitive signals does not prove
that they are actually used for spatial perception. What has
been lacking in the study of the neural computations that
underlie the fusion of these touch and motion signals is a
vibrissa-mediated behavior that requires sensorimotor integration. One such task would ask if a rat can use its vibrissae
to differentiate between objects that differ only in rostrocaudal angle, i.e., azimuthal angle or angle along the
rostrocaudal sweep of the vibrissae. However, the nervous
system could in principle ignore motor information and solve
this problem using the topography of the vibrissa array.
When the motion of the vibrissae is comparable to their
separation, the rostrocaudal position of an object can be
judged from the peripheral origin of the touch signal (Figure
1A), in a scheme known as labeled-line encoding [30]. In this
representation, the topographic identity of the cortical
region activated by contact corresponds to object location,
because each region of space is only scanned by a single
sensor. An animal could thus use its vibrissa array to
discriminate object angle if it used large-amplitude, exploratory motion to detect an object and switched to smaller
motion for localization.
In the more typical exploratory whisking motion [31–34],
vibrissa sweeps overlap, and the angular location that
corresponds to contact requires information beyond the
identity of the contacting vibrissa (Figure 1B). In this case, the
presence of position-sensitive neurons suggests that the
position of the vibrissae at the time of contact could provide
context to interpret the contact event [35,36]. This sensorimotor approach falls under the rubric of haptic perception,
as it is based on the awareness of the position of ‘‘an object
relative to the body and the body relative to an object’’ [1].
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Figure 1. Two Localization Algorithms: Topographic Labeled-Line and
Haptic-Sensing
Each cartoon depicts an animal contacting a small object (black circle)
and an idealization of the resulting neural streams (dashed arrows)
afferent to the vibrissa somatosensory cortex.
(A)A labeled-line strategy. During small motion, the location of an object
is encoded in the identity of the vibrissa that contacts it. For clarity, only
one row of vibrissae is shown; additional rows do not directly aid
localization.
(B)A sensorimotor strategy. During large motion, contact on a given
vibrissa leaves object position ambiguous. Information about the
position of that vibrissa at the time of contact resolves the confound.
This scheme does not require multiple vibrissa.
doi:10.1371/journal.pbio.0050015.g001
Other algorithms derived from the touch sensation, such as
duration of contact [28], are possible if different object
positions result in reproducible differences in the structure
of the contact event [37]. These approaches share the
common feature that they do not depend on vibrissa identity
and, therefore, unlike the labeled-line scheme, could be
performed with a single vibrissa. To differentiate between
these possibilities for spatial encoding and relating known
sensorimotor physiological signals to a sensorimotor behavior, we thus ask if behaving rats are able to discriminate
between objects at different rostrocaudal angles when
restricted to the use of a single vibrissa.
Results
We tested 14 rats in an angle-based spatial discrimination
task by using an apparatus designed for semi-automated
training (Figure 2). Briefly, each animal was assigned two
stimulus positions whose rostrocaudal angles differed by 15 8.
One of these positions was designated the rewarded, or Sþ,
stimulus, and the other position was designated unrewarded,
or S. The animal performed a series of trials in which it
maintained a fixed head position while presented with a thin
rod at one of these two positions. Under a go/no-go paradigm
with a fixed ratio reinforcement schedule [38], the animal was
required to respond to the Sþ position with a block of L lever
presses within T seconds after stimulus presentation to obtain
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Figure 2. Apparatus for Behavioral Testing and Training
(A) View of training arena. Animals were placed in the vestibule at the start of a session, and their position was monitored through infrared sensors. The
U-shaped restraint bar blocked the tunnel while allowing access to the operant lever and nose poke. Discrimination trials started when an animal
interrupted the nose poke sensor, causing either the rostral or caudal stimulus pin to descend into the vibrissa field. The stimuli were translated by airdriven pistons and positioned through a circular guide fixed relative to the nose poke (supporting parts omitted for clarity; see Figure S4). Lever presses
in response to the Sþ stimulus, either rostral or caudal for each animal, were rewarded with a drop of water in the fluid dispenser. Any remaining fluid
was withdrawn by vacuum at the end of the trial. An infrared lamp provided backlit contrast of the head and vibrissa for the camera recording the
ventral view shown in (C). The entire arena was enclosed in a darkened, sound-attenuated chamber (not shown).
(B) Detail of stimulus area from (A).
(C) View of stimulus area from (A), as seen by the camera. The nose poke allowed reproducible positioning of the stimuli in head-centered coordinates
(see also Figures 6A, 6B, 6D, 6E, and S1).
[Original artwork: Jenny Groisman]
doi:10.1371/journal.pbio.0050015.g002
a fluid reward (see Methods); we used T ¼ 8 s. Lever presses in
the S condition were recorded but had no consequences. An
animal was considered to discriminate between the two
positions when multiple consecutive sessions showed a
statistically significant difference between Sþ and S trials in
the latency to complete this block response. We trained
animals on this task with their full complement of vibrissae
and then tested them while removing vibrissae, first down to a
single row and finally to a single vibrissa.
We considered it likely that a typical rat has the perceptual
ability to perform this single vibrissa discrimination, despite
the fact that only five of our initial 14 animals showed
consistent behavioral differences between Sþ and S trials
when tested with a single vibrissa (Figure 3). This attrition was
largely due to a weakness in the behavioral measure used early
in the study. The majority of the animals who did not progress
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to the single vibrissa condition were tested with a minimal
lever press response requirement, L ¼ 1 (Figure 3; animals
outside the dashed box did not succeed in the single vibrissa
task and animals with numbers in gray were tested with L ¼ 1).
The lack of demonstrated discrimination for these animals
was likely because the low response requirement did not
discourage animals from responding when they were able to
predict that no reward would be forthcoming [38]. We thus
raised the response requirement on L for later animals until
differences in Sþ and S responses were seen (L ¼ 4–6), and we
then reliably measured discrimination for testing with all
vibrissa intact (Figure 3; animals with numbers in black). This
large increase in training success rate suggests that the
measurements were limited by our ability to motivate the
desired behavior rather than the animals’ perceptual abilities.
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confidently measure a difference in the average response to
Sþ and S stimuli for this animal within 0.5 s of stimulus
delivery.
The time in which these two response profiles diverge
included the intervals needed both to form a sensory percept
and to emit at least one lever press, i.e., tdiverge ¼ tperception þ
tmotor. To place an upper bound on the interval tperception
needed for active sensing alone, we estimated the minimum
time tmotor required for the motor act of pressing the lever
from two observations. First, the slope of the linear part of
the cumulative response for Sþ trials gave the mean response
rate during sustained responding. This rate was roughly 2.5
lever presses per second, or 400 ms per average lever press
(e.g., Figure 4B). Second, the shortest time taken by any
animal to reach L ¼ 5 lever presses was roughly 1.5 s (e.g.,
Figure 4C). Because few responses occurred in the first 250 ms
of a trial (e.g., Figure 4A), this left 1.25 s for five lever presses,
or 250 ms per lever press in the fastest cases. Both measures
were based on blocks of lever presses that did not require
further decision-making by the animal, and thus isolate the
time tmotor to be 400 ms for typical responses and 250 ms for
the fastest responses. Given tdiverge ¼ 500 ms and using tmotor
250 ms, these data demonstrate that the complete interval
tperception required to detect the stimulus and form a percept
of stimulus position is less than 250 ms.
Variability across Sessions and Animals
The latency to reach the total required number of
responses L in each trial served as our primary measure of
behavioral discrimination (Figures 4C and 5A). A given
session was considered to demonstrate stimulus discrimination when the Sþ and S latency distributions significantly
differed, as measured by a two-sided Kolmogorov-Smirnov
(K-S) test. Consistent with the lack of an overt penalty in S
trials, we observed many more false-positive (type I) errors—
where an animal completed L lever presses with short latency
during an S trial—than false-negative (type II) errors
(Figures 4C, 5A, and 5B). Since the K-S statistic does not
provide information about the types of errors, we confirmed
consistent performance over multiple sessions by plotting
receiver operating characteristic curves [39] for the detection
of the Sþ stimulus (Figure 4D). Each receiver operating
characteristic curve shows the dependency between false
positive trials, i.e., S trials with latencies shorter than a
threshold s, and true positive trials, i.e., Sþ trials with
latencies shorter than s, as the latency threshold s is varied.
Loosely, a steep slope near the left side of the graph indicates
few type I errors, whereas a shallow slope near the right side
of the graph indicates few type II errors; the integrated
distance to the diagonal is a measure of the overall
discriminability of the two distributions. The numbers of
type I and type II errors fluctuated between sessions, but all
animals showed a tendency for false-positive errors.
Further, although the bimodal nature of the latencies
(Figure 4C) was consistent for all five animals in the single
vibrissa task, the time at which Sþ and S responses diverged
fluctuated across sessions and animals. Each of the three
animals that passed all controls, as described below,
performed sessions in which the average Sþ and S responses
diverged within 650 ms. The remaining two animals took
longer, i.e., greater than 1,000 ms, due to the head-turning
behavior that is described below. These response times are
Figure 3. Summary of Performance Levels Achieved for All Animals
Each row represents one of 14 rats tested on the spatial discrimination
task. The first column gives an identifying number, and the second
column gives the corresponding Sþ stimulus assignment (R for rostral
and C for caudal). Animals with gray numbers were tested with response
requirement L (Figure 7D) set to 1, and the remaining animals were
tested with L ¼ 4–6. The next three columns summarize performance as
the number of intact vibrissae decreased. Filled circles indicate stable
performance at a given level, and open circles imply that an animal was
tested but did not achieve stable performance. ‘‘Stable performance’’ is
defined here as statistically significant differences in Sþ and S responses
over multiple sessions. In two cases, rat number 8 and rat number 12,
external circumstances caused the end of testing despite success at all
attempted stages. The final column describes testing under various
control conditions, and filled circles here indicate that a given animal
passed all controls. The dashed box highlights those animals that
succeeded in the task when limited to a single vibrissa. Among these
rats, those that habitually sampled the stimuli with their head are shown
with half-filled circles in the control column, since it was unclear whether
this movement was involved in forming a spatial percept.
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Time Scale of Single Vibrissa Discrimination
We compared the pattern of lever presses between Sþ and
S trials to estimate the time required to form a behavioral
decision. Since the presence or absence of a reward after L
lever presses could be used to distinguish the two stimulus
conditions (Figure 4A), we considered only the first L
responses in each trial in our analysis. The cumulative
response count, averaged separately for Sþ and S trials,
quantified this time course for a given session (Figure 4B). Sþ
trials resulted both in a higher response rate and in a lower
latency to response onset relative to S trials. In a typical
session for the animal with the fastest responses (Rat number
20), the average response counts for the two conditions began
to diverge approximately 250 ms after the start of a trial, and
the 95% confidence regions became permanently nonoverlapping after 500 ms (Figure 4B; gray arrows). Thus, we could
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cumulative lever press counts for Sþ trials; equivalent data for S trials
are in red. The gray arrows at 0.5 s mark the time point after which the
2r error regions remain nonoverlapping.
(C) Distribution of latencies from the start of a trial to the fifth lever press,
for the trials shown in (A). Trials with fewer than five responses are
shown at infinite latency. The bars and left ticks show numbers of trials
as a function of latency, and the lines and right ticks show the same data
as cumulative distributions. The Sþ and S distributions are statistically
distinct (p , 0.001, two-sided K-S test). Green indicates Sþ and red
indicates S.
(D) Receiver operating characteristic curves summarizing differences
between Sþ and S latency distributions for multiple sessions. The
fraction of Sþ trials with latencies below a threshold s is plotted against
the fraction of S trials with latencies below the same s; the curves are
then constructed as s varies parametrically. The result for the data from
(C) is shown by the solid black line, where the heavy part of the line
corresponds to the threshold s having traversed the heavy parts of the
lines in the inset data. The gray lines are from 12 subsequent single
vibrissa sessions by the same animal (rat number 20). The orange line
corresponds to the control session from Figure 5C. Identical Sþ and S
response distributions would yield the diagonal dashed line.
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consistent with an estimate of 250 ms for time needed for
spatial discrimination.
Finally, the experimenter-defined association of stimulus
position with reward condition varied across these five
animals. Although all single vibrissa trials were performed
at an angular separation of 15 8, the animals were tested on
different absolute stimulus positions. For example, rat
number 20 was tested with vibrissa C1 for Sþ set to þ15 8
and S set to 0 8, and rat number 9 was tested with vibrissa C2
for Sþ¼7.5 8 and S¼þ7.5 8. In total, two animals had rostral
Sþ assignments, and three had caudal Sþ assignments. We did
not find any gross differences in training time or performance correlated with these parameters, which suggests that
the absolute position of the Sþ and S stimuli did not play a
role in the discrimination.
Controls
For the five animals that succeeded in the single vibrissa
task over multiple sessions, we carried out three controls to
verify that discrimination derived solely from vibrissamediated tactile cues. We first tested for visual cues. Although
behavioral testing occurred in a dark chamber, a highintensity infrared lamp with a peak wavelength of 850 nm was
used for videography. We considered it possible, though
unlikely [40], that residual visible light from this lamp was
available to the animals. We thus tested performance in
sessions for which the lamp was turned off, as illustrated by
the data of Figure 5B. None of the five tested animals lost the
ability to perform the task in the absence of the infrared
illumination.
We next tested for a contribution from head movements.
Stimuli were delivered after an animal fixed its head position
in the nose poke and were retracted when fixation was lost
(Figure S2); but mechanical lags created an approximately
150-ms window after an animal left the nose poke during
which the stimulus was not fully retracted. Video observation
showed that two of the five animals that succeeded in
discrimination with a single vibrissa habitually probed the
stimuli with their snouts after making vibrissa contact. It was
not clear whether this movement was needed to aid stimulus
localization, or whether it occurred as a reflex motion after
the location had already been judged. Since we could not rule
out the former possibility, we considered these cases
ambiguous (Figure 3; half-shaded circles).
Figure 4. Temporal Profile of Behavioral Responses for One Session
(A) Lever press responses in a session by rat number 20 restricted to the
right C1 vibrissa. The trial length T was 8 s and response requirement L
(Figure 7D) was five lever presses. Each row shows the first five lever
presses in one trial, with responses from Sþ trials in green and those from
S trials in red. The fifth response in an Sþ trial was followed by a reward.
This session consisted of 58 Sþ trials and 56 S trials over 30 min.
(B) Cumulative lever press counts from (A), averaged separately over Sþ
and S trials. The inset illustrates this data transformation. The green line
and shaded region give the mean 6 2r (standard error of mean)
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We finally tested the remaining three animals for the use of
auditory and vibrational cues. The pistons used to deliver the
stimuli were damped to reduce vibrations, and testing was
carried out in the presence of an audio mask to interfere with
any sound differences in Sþ and S stimulus delivery. To
confirm that discrimination was not based on residual
indirect cues arising from stimulus motion, each animal was
tested in a session where the pistons functioned as usual but
the stimulus pins were absent. A resulting degradation in
performance indicated that tactile contact with the vibrissa
was required (see Figure 5C and the orange line in Figure 4D).
None of the three tested animals showed significant discrimination in these control sessions.
In several sessions, we were able to further control for
vibration cues by restricting our attention to trials in which
the animal broke fixation less than 250 ms after the start of a
trial. In these cases, the stimulus was retracted before it fully
entered the vibrissa field (Figure S2). This allowed the pistons
to travel over nearly their entire range but left insufficient
time for the vibrissae to encounter the stimuli. In sessions
with sufficient numbers of these ‘‘jump-the-gun’’ trials, we
verified that discrimination performance was at or near
chance with this limited opportunity for vibrissa contact, as
seen in Figure 5D.
Whisking Strategies
To characterize the formation of the spatial percept in the
interval tperception preceding the motor response, we made
high-speed infrared video recordings of vibrissa motion for
two of the three animals that passed all of the controls, i.e., rat
number 9 and rat number 20 (Figure 6A, 6B, 6D, and 6E).
Vibrissae positions estimated from these recordings typically
showed a slow drift until approximately 100 ms into the trial,
followed by larger-amplitude, but often nonsinusoidal,
vibrissa motion on a changing baseline (Figure 6C and 6F).
This interval reflects the delay after the stimulus begins to
descend before the animal realizes that a trial has begun.
Thus, further subdividing tperception ¼ tdelay-to-start-of-search þ
tactive-sensing yields an estimate for the average time required
to actively scan for a stimulus as tactive-sensing ’ 150 ms.
Constraints on sensorimotor algorithms can be obtained
from a more detailed analysis of patterns in the vibrissa
motion. An animal could adopt a purely motor strategy by
repeatedly positioning its vibrissa in the expected location of
one of the stimuli and then simply detecting contact. To rule
out this approach, we examined the distribution of all vibrissa
positions in the first 250 ms of the trials, an interval chosen
because it included few stimulus contacts. This distribution
was, in all cases, centered between the two stimuli, indicating
that vibrissa positions spanned both potential locations
rather than habitually preferring one (Figure 6G). In a
related strategy, an animal could center its vibrissa between
the Sþ and S stimulus locations and then associate contact
during protraction with the more rostral stimulus and
contact during retraction with the more caudal stimulus. As
a test of this directional bias, we calculated the velocity of the
vibrissa just before contact with Sþ and S stimuli. Contact at
each location occurs during both protracting and retracting
movements, so that the direction of contact does not encode
stimulus location (Figure 6H). This is consistent with the
further observation that the distribution of vibrissa positions
in the first 250 ms of the trials extends beyond the location of
Figure 5. Controls for Extravibrissal Cues
(A) Latency distributions for a standard session, performed by rat number
20 and similar to Figure 4C. This session contained 54 Sþ trials and 51 S
trials and showed a significant difference in the latency to the
completion of a five–lever press response requirement when comparing
responses from Sþ and S trials (p , 0.001, two-sided K-S test).
(B) A session performed without infrared (IR) illumination. This session
contained 45 Sþ trials and 54 S trials and showed a significant
difference between Sþ and S response latencies (p , 0.001, two-sided
K-S test).
(C) A session in which the stimulus pins were absent. This session
contained 21 Sþ trials and ten S trials and showed no significant
difference between Sþ and S response latencies (p . 0.1, two-sided K-S
test). The number of trials was smaller here because the animal
performed trials at a lower rate in this condition, and because the
session was short (15 min versus 30 min above) to prevent extinction of
the discrimination behavior.
(D) Data from the session shown in (A) above, restricted to trials in which
the animal broke fixation before the stimulus had fully extended. This
condition included seven Sþ trials and ten S trials and showed no
significant difference between Sþ and S response latencies (p . 0.1,
two-sided K-S test).
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Figure 6. Patterns of Vibrissa Motion during Discrimination
The data in (A) to (F) are from the session analyzed in Figure 4, with Sþ stimulus (rostral for rat number 20) at þ158 and S stimulus at 08. The scale bar in
the photographs is equal to 4 mm.
(A) Projection of 400 frames from a single Sþ trial. This image shows the range of vibrissa positions in the interval from 0.5 to þ1.5 s relative to the start
of a trial; this range arises from whisking movements as well as small head motion and translations of the mystacial pad. The Sþ stimulus neighborhood
is indicated by a green box, and the S stimulus region is in red. The dark line in the green box is due to stimulus motion; compare to the green boxes
in (B) and (E), which show fully extended and retracted positions, respectively. Stimulus displacement appears smaller than the true 5-cm travel because
the motion was nearly normal to the focal plane (Figures 2A and 2C).
(B) Single frame in which the vibrissa contacted the Sþ stimulus, taken from the trial in (A). The blue rectangle indicates the region in which vibrissa
position was estimated for (C).
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(C) Vibrissa position as a function of time. The green and red bands correspond to the vertical extent of the similarly colored boxes in (A). The gray lines
give position traces from 58 Sþ trials, and the black line highlights the trial shown in (A). The stimulus is not seen here, but both rostral and caudal
stimuli started their descent at ;30 ms and reached full extension at ;300 ms (Figure S2). The stimuli were fully withdrawn within 150 ms of the end of
nose poke fixation; this occurred at a median of 315 ms for Sþ trials and 530 ms for S trials. The green arrow marks the Sþ contact in (B), and the
dashed black line demonstrates the ;100-ms delay in the onset of whisking after the start of a trial. Breaks in the lines are due to tracking errors.
(D and E) Video images from an S trial, analogous to (A) and (B).
(F)Vibrissa position traces for 56 S trials, analogous to (C). The red arrow marks the S contact in (E).
(G) Summary of all tracked vibrissa positions from 0–0.25 s after the start of each trial, including both Sþ and S trials. The green and red bands
correspond to the vertical extent of the corresponding regions in (A) and (C) and show that the vibrissa scanned both stimulus positions. The thick line
is derived from the session analyzed in (A) through (F). The thin lines are taken from five more sessions by rat number 20 and four by rat number 9;
these lines were scaled to align with the Sþ and S bands drawn for the session represented by the thick line.
(H) Precontact vibrissa velocities. Bold lines show the distribution of angular velocities as the vibrissa approached the stimulus for all contacts from (C)
and (F), excluding intervals in which the vibrissae were in contact with a stimulus and thus not appreciably moving (defined as a velocity 1 pixel per 5
ms frame). The thin lines are taken from the sessions considered in (G). In each case, the Sþ and S stimuli are associated both with contacts of positive
velocity (i.e., retraction) and of negative velocity (i.e., protraction). Data from Sþ trials are in green and data from S trials are in red.
(I) Vibrissa contact event durations. Bold lines show the distribution of all contact durations from (C) and (F). The thin lines are taken from the sessions
considered in (G). The traces vary in the width of the early peak and the fraction of sustained contacts, but none shows marked differences between Sþ
and S distributions. Sþ contacts are in green and S contacts are in red.
doi:10.1371/journal.pbio.0050015.g006
variability in performance may have obscured indications of
subtle changes in strategy.
The time scale for tactile search was estimated from the
measured behavioral delays. Animals could selectively initiate
a motor response in as little as 250 ms after the start of an Sþ
trial (Figures 4B, 4C, and S3). In this short interval, we
typically observed delays of 100 ms from the start of a trial
before the vibrissa started a large amplitude scanning motion
(Figure 6C and 6F). Taken together, these intervals imply that
the time tactive-sensing including the entire sensorimotor
process of motor scanning, object detection, and spatial
categorization can be as short as 150 ms. Given a typical
frequency of exploratory whisking in the range of 7–15 Hz
[33], this suggests that no more than one to two whisk cycles
were sufficient to judge position. Although the animals in our
study often did not show the highly sinusoidal vibrissa motion
found in other studies [33,43], perhaps due to the physical
restriction of the nose poke, the observed time scale of
vibrissa motion here is consistent with these frequencies.
the two stimuli (Figure 6G), so that contacts can occur in both
movement directions.
Another class of algorithms that does not require integration of positional and contact information depends on the
duration of vibrissa contact [28,37,41]. For periodic vibrissa
motion, the time between contact onset and offset could be
transformed into object position. Such a scheme might be
accomplished more generally for any vibrissa motion in
which contact duration is a monotonic function of vibrissa
angle. We thus asked if the distribution of contact event
durations was different for Sþ and S trials. These contacts
were largely brief events of less than 50 ms, although
extended contacts of greater than 300 ms occasionally
occurred (Figure 6I). This overall distribution of contact
durations is consistent with earlier measurements (Figure 3A
from Sachdev et al. [42]) but the precise times varied broadly
from trial to trial. Thus, for all animals, the variability of
contact duration was large relative to any separation between
the peaks of the distributions for the Sþ and S conditions. In
light of this variability, we consider an algorithm based on the
duration of contact unlikely to account for the observed
behavioral performance.
Neural Algorithms
Earlier studies have suggested the calculation of dorsoventral angle from the identity of the contacting row [41,44] and
demonstrated discrimination of distance from contact with
multiple vibrissae, even in the absence of active whisking [21].
We focused here on the decoding of angle along the axis of
vibrissa motion because of the confound arising from that
motion, i.e., the environmental meaning of exteroceptive
tactile signals changes as an animal moves its vibrissae. Given
that this computation can be accomplished using the
information associated with a single moving sensor, we
consider the algorithms that might be used to transform a
contact signal into a spatial position.
A purely motor strategy could have taken advantage of the
fixed stimulus locations in our task design. Because only two
positions were possible, an animal might learn to focus its
now sparse sensory apparatus on one of these two positions
and use the presence or absence of a contact event to detect
the Sþ (or equivalently, S) condition without considering
both sensory and motor cues. This is a single vibrissa
approximation of a labeled-line strategy (Figure 1A), which
requires motor control sufficient to hold a lone sensor near
an expected target. This approach was ruled out by the
motion patterns of the vibrissa; in both animals for which we
tracked vibrissa position, the scanning motion was not
restricted to the region of a single stimulus (Figure 6G). At
Discussion
We have demonstrated that rats with a single vibrissa can
respond to differences in the position of external objects that
differ only in angle along the direction of vibrissa motion. A
rat with a full array of vibrissa could in principle perform this
task by limiting vibrissa motion to nonoverlapping fields and
by using the collection of vibrissa columns, or arcs, as a spatial
sensory array to test multiple locations in parallel (Figure 1A).
The ability of animals to identify spatial angle when restricted
to a single vibrissa argues that this sensorimotor system is
able to determine the position of contact with an object while
serially scanning a single sensor. The motion of the vibrissae
as the animals performed this task was observed to span both
stimulus locations prior to contact (Figure 6G), make contact
during both protraction and retraction (Figure 6H), and
remain in contact with both Sþ and S stimuli for similar
durations (Figure 6I). Although these experiments did not
focus on discrimination using multiple vibrissae, we note that
animals did not show any marked change in strategy or
accuracy as they transitioned from single row to single
vibrissa testing. This suggests that animals used the scanning
strategy with multiple vibrissae as well, but the large
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(D) Stimulus discrimination testing. The audio prompt was eliminated
from Sþ trials. The number of lever press responses, L, required to obtain
a reward in Sþ trials was increased until a difference between Sþ and S
responses was apparent. This value was typically L ¼ 5 or 6; the example
here illustrates L ¼ 2. The structure of S trials was unchanged.
doi:10.1371/journal.pbio.0050015.g007
the opposite extreme, the wealth of sensory information
available from the vibrissa follicle suggests a purely sensory
strategy that might arise from differences in the nature of
contact as a function of position. The existence of separate
on- and off-contact touch signals [28] allows for the
possibility that the nervous system determines the duration
of a contact and converts it into a spatial position, especially
for cases such as sinusoidal motion where different positions
result in characteristic contact durations. This temporal
delay scheme is contraindicated by the similarity of the
measured contact durations (Figure 6I). Finally, a strategy
that uses both sensory and motor signals, but with low
resolution, would be to position a vibrissa such that it
approaches the two stimulus positions from different
directions, e.g., during protraction versus retraction. The
measured broad heterogeneity of velocity approaching
contact (Figure 6H) makes it unlikely that such gross
directional cues encoded stimulus position.
The most parsimonious remaining explanation for the
computation needed to derive spatial position from a contact
event is the integration of touch with kinesthetic information
about the location of the vibrissa at the time of contact.
Although there is no evidence of proprioceptive muscle
spindles in the mystacial pad [45], physiological studies have
shown that a reafferent motor signal from the pad is present
at levels from the trigeminal ganglion [28,46] to thalamic
nuclei [47] to primary somatosensory cortex [26,29,48,49].
The evidence described here argues that this positional
information can be used behaviorally as a reference against
which to interpret sensory contact, informing spatial perception of objects near the head. Preliminary electrophysiological data show how the fusion of these two signals can
occur in the brain [50].
Previous theoretical studies have taken advantage of the
rhythmic nature of exploratory whisking to suggest neuronal
circuits that might compute spatial location given periodic
spike trains representing both contact and vibrissa motion
[36,51–53]. The mathematical formulation of this class of
algorithm, however, requires multiple rhythmic whisk cycles
to establish a phase reference. The animals in our study and
another study with head-restrained animals trained to touch
objects with their vibrissae [54] do not appear to precede
contact with periodic whisking (Figure 6C and 6F) (Figure
3A of Sachdev et al. [54]). This ability to form a spatial
percept from oscillatory but irregular vibrissa motion,
within one to two cycles after whisking onset, argues against
mechanisms that depend on periodicity. A more-direct
circuit that performs the same computation would compare
spiking in contact-sensitive and position-sensitive cells of
varying preferred position. Ongoing physiological studies
characterizing these neuronal interactions suggest that this
comparison can in fact integrate tactile and haptic streams
[50]. Finally, a last constraint on any proposed neuronal
implementation of a spatial decoding algorithm should at
least account for resolution sufficient to distinguish contacts
separated by 158. Directed studies of the threshold for
Figure 7. Behavioral Logic for Operant Training and Discrimination
Testing
All diagrams use 0.5-s intervals here for clarity; the actual sampling rate
was 16 Hz.
(A) Lever press response training. Animals that waited D seconds without
emitting a lever press would elicit an audio prompt that signaled the start
of a trial. The first lever press response in the following T¼6 s was rewarded
with a drop of water. At the end of the trial, any remaining water was
withdrawn. D was increased from 0.25 s to 4 s.
(B) Nose poke training. D was first increased from 4 to 60 s to decrease
the frequency of trial initiated by waiting. Trials could alternatively be
initiated if an animal placed its nose in the nose poke for N seconds. As
this behavior was established, N was increased from 0.063 s to 1.5 s.
(C) Stimulus training. All trials in this stage were initiated by a 1.5-s nose
poke. Each trial was randomly assigned as either Sþ or S, and the start
of the trial was signaled by the descent of the corresponding stimulus
pin. The pin remained in the vibrissa field until nose fixation was broken
or until the trial ended. In Sþ trials, the first lever press response after the
start of the trial resulted in a reward. If no response occurred within P
seconds, an audio prompt sounded. P was increased from 0.125 s to 6 s.
Lever presses were ignored in S trials.
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speaker to deliver sound cues, an auditory white-noise mask, a
SecuraCam infrared camera (Swann [http://www.swann.com.au]) for
monitoring by the trainer, and a low-flow gas line to ensure
breathable air. The area available to the animal consisted of an
acrylic vestibule, 200 mm on a side, and a 200-mm long 3 57-mm
inner diameter tunnel, both placed on an acrylic shelf elevated 60
mm above the floor of the external enclosure. Motion through the
tunnel was registered by an 880-nm infrared photodiode (PhotonicDevices, PDI-E802 [http://www.photonicdevicesinc.com])/phototransistor (DigiKey, QSE156-ND [http://www.digikey.com]) pair to signal
the presence of a rat. The end of the tunnel was fitted with a Ushaped restraint bar that allowed free movement of the head and
paws while preventing escape (Figure 2B).
Behavioral output was measured through a water-sealed lever of
25-g activating force (Cherry E73-series switch, DigiKey, CH566-ND),
affixed with a plastic crossbar, and placed at the end of the tunnel
(Figure 2B). Animals typically rested on the crossbar and activated the
lever by briefly raising their paws; early in training, a small spring was
often placed to aid this motion. Fluid rewards were delivered to a sip
cup cut into a stainless steel dispenser, placed ; 60 mm from the end
of the tunnel and designed with inflow and outflow ports to control
the timing of fluid delivery. Fluid was delivered in 50-ll aliquots
through a miniature direct current solenoid valve (Parker-Hannifin,
004-0008–900 [http://www.parker.com]) with a custom timer circuit
(University of California at San Diego Physics Electronics Shop) to
gate flow from a reservoir and then removed by a similarly controlled
solenoid gating a vacuum line. A bright yellow light-emitting diode
(587 nm, 1,900 mcd, Radio Shack 276–351 [http://www.radioshack.
com]) was wired in parallel with the reward timer to indicate reward
availability and interfere with visual dark-adaptation to any residual
light in the chamber, e.g., from the camera illumination lamp. This
entire fluid delivery system was flushed with enzymatic detergent
(MaxiZyme, Henry Schein, #10–7410 [http://www.hsa.ca]) after each
training session to prevent build-up of organic solids. This cleaning
step was particularly necessary early in the training when chocolate
milk was sometimes used as a liquid reward.
Rat head position was fixed by a 13-mm outer diameter brass nose
poke cone, painted black to minimize stray reflections, with an analog
reflective infrared sensor (940 nm, DigiKey, QRD1114-ND), whose
output was taken to an analog comparator (LM319N, DigiKey, 4971577–5-ND). The comparator was wired as a Schmitt trigger and
referenced to a potentiometer adjusted to control nose poke
sensitivity. The nose poke was placed close to the fluid dispenser
and fixed relative to the stimulus with an aluminum bracket (not
shown in Figure 2; see Figure S4). This system allowed some positional
ambiguity, as an animal could roll its snout freely while maintaining
fixation. However, translational position was reproducibly constrained (Figures 6B, 6E, and S1).
Digital inputs taken from the lever, tunnel sensor, and nose poke
sensor were sampled at 16 Hz by a multifunction digital input/output
board (National Instruments, AT-MIO-16DE [http://www.ni.com]) in a
personal computer running custom LabVIEW software (National
Instruments). The software logged the inputs, implemented training
logic, and supplied digital control signals for the reward, vacuum, and
stimulus valves.
Tactile stimuli. The stimuli for the spatial task were 0.86-mm steel
rods translated into and out of the vibrissa field by a custom airpiston and guide assembly (Figure S4). Two paired Lexan guide blocks
were aligned on Teflon-coated shafts (15 cm long 3 0.6 cm deep,
McMaster-Carr, 7875K11). The floor of the bottom guide rested on
plastic legs 110 mm above the floor of the tunnel. These legs, the topguide, and the alignment shafts (Figure S4) were left out of Figure 2A
for clarity. A carriage block (Figure S6B) with a captured linear
bearing was free to slide on the two rostral shafts, and a mirror-image
block traveled along the two caudal shafts. Two stainless-steel air
cylinders (spring-return, 5-cm travel, McMaster-Carr, 6498K27) were
fixed to the top block (Figure S6A), each with its piston bolted to one
of the carriage blocks. Air at 140 kPa was delivered to the pistons
through a pair of three-way miniature solenoid valves (ParkerHannifin, 004-0008–900) that were placed outside of the enclosure to
minimize noise. These valves were connected to 12 V direct current
supplies via power transistors (Mouser, 610–2N6387 [http://www.
mouser.com]) for digital control. Inflowing air was passed through a
restriction valve, common to both stimuli, which was adjusted to slow
piston descent and minimize vibration during stimulus delivery.
Outflowing air was similarly restricted, and silicone bumpers were
placed between the carriage and guide blocks to damp vibration from
the sudden deceleration at the ends of travel. The resulting stimulus
descent and ascent took ;250 ms and ;150 ms, respectively, for the
full 5-cm travel, including an approximate 30-ms delay in both cases
absolute angular discrimination are required to establish the
psychophysical limits of spatial acuity, as has been done for
the bilateral comparison of distance [21] and angle [55].
The Vibrissa System and Sensorimotor Integration
Our behavioral task was designed to isolate a sensory
process that is ordinarily used in concert with other behaviors.
Earlier studies involving spatial behaviors support the notion
that the vibrissae serve as binary detectors in freely exploring
animals [20], and this may be the ethologically more typical
usage when an animal can orient its head following contact.
Indeed, upon detection of the salient and asymmetric stimulus
used in this study, some animals in our study reflexively
oriented to explore the stimulus further, perhaps bringing
their microvibrissae to bear. Although we could not determine
whether those animals had judged stimulus position before
orienting, we note that refined rostrocaudal information is
necessary if a rat is to orient rapidly following contact without
further search. Although the current study does not attempt
to characterize the role of angular perception during natural
activity, we note that the vibrissae are involved in activities
with complex spatial demands, such as navigation [14,44],
aggression [56], and swimming [57] (for a general review of the
classic literature, see Gustafson and Felbain-Keramidas [7]).
This ubiquitous role suggests that these sensorimotor organs
paint a richer picture of the tactile world than would be
possible from binary detection alone. When taken with recent
work on the role of the vibrissae in the transduction of fine
texture [10–13], the proportionally large neural territory
given to vibrissa processing emerges as the potential locus of
integration for multiple modalities.
A practical advantage to the study of integration processes
in the vibrissa system lies in the large body of work on the
plasticity, anatomy, and sensory response properties [36,58–
62] related to the vibrissa primary somatosensory or barrel
cortex. A variety of recent studies take advantage of this
growing body of literature and use the vibrissa system to
develop modern experimental methodologies [63–65]. In
recognition of the requirements of these techniques, our
choice of a go/no-go paradigm, rather than a two-alternative
forced choice design [66], was in part motivated by the hope of
eventually measuring behavior in animals head-fixed for
imaging or intracellular studies [29,63,67–69]. The present
work demonstrates that rats can use this popular model system
to integrate feed-forward sensory events with motor feedback
to inform their model of the external world. The elucidation
of the circuitry that performs this computation will bring us a
step closer to understanding how sensorimotor loops derive
the perception of space from the sensation of touch.
Materials and Methods
Our initial cohort of behavioral subjects consisted of 24 LongEvans rats, 14 of which reached the stimulus training stage of the
study (Figure 3). All of these animals were females of 100–200-g mass
at the start of training. All procedures involving animals conformed
to National Institutes of Health guidelines and were approved by the
Institutional Animal Care and Use Committee at the University of
California at San Diego (La Jolla, California, United States).
Training apparatus. Animals were trained and tested in a custom
operant arena (Figure 2A). The arena was contained in an enclosure
760 mm 3 500 mm 3 420 mm (not shown in Figure 2) made of 1/4-in.
(0.6-cm) acrylic and padded with skinned polyether foam (1 in. [2.54
cm]; NRC 0.8, McMaster-Carr, 5692T49 [http://www.mcmaster.com])
to dampen external sound and light. The enclosure contained a
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to increment task difficulty, and a large part of training occurred
without further experimenter intervention. The parameters used in
Figure 7 and in the description below are: T, trial length; D, delay
between trials; N, duration of nose fixation; P, delay until audio
prompt; and L, number of lever press responses required to obtain a
reward. P and L were used in rewarded stimulus trials only.
The first stage defined the lever response and brought it under
experimental control (Figure 7A). In this stage, animals were required
to be in the tunnel without emitting lever press responses for an
interval of D seconds to elicit an audio prompt, i.e., 300 ms at 2 kHz,
which indicated the start of a trial. The first lever press response
within T seconds following the prompt was rewarded with a 50-ll
reward, signaled by a light-emitting diode indicator as described
above. At the end of T seconds, the trial ended, and any water still in
the dispenser was removed by vacuum. This schedule encouraged
early responses relative to the audio prompt, because responses that
were late but still within T seconds after the prompt afforded less
time to drink. The trial length T was set here to 6 s, and the delay
parameter D was increased from 0.25 s to 4 s. Human intervention
was often necessary in the first several sessions to model the lever
press response, but was minimal as D increased.
The second stage shaped the nose fixation behavior (Figure 7B).
Here, the D parameter from stage 1 was increased from 4 s to 60 s, so
that the audio prompt was more difficult to elicit by waiting alone. As
before, the first lever press response within T ¼ 6 s of the prompt was
rewarded. A nose poke response of duration N seconds shortcircuited this delay and immediately caused the start of a trial. The
nose fixation duration N was increased from 0.063 s to 1.5 s in
increments of 0.063 s. Acquisition of the basic nose poke behavior
was assisted by increasing the sensitivity of the nose cone sensor and
baiting the nose cone with water or chocolate milk; after this
acquisition, little intervention was required as the fixation duration
parameter N was increased.
The third training stage transferred the reward context from the
audio prompt to one of the two stimuli in a go/no-go task (Figure 7D).
Each animal was randomly and permanently assigned a relative
position, either more rostral or more caudal. For each session, the
tactile stimulus that occupied this relative angular position was
designated Sþ, as opposed to the S stimulus at the second position.
In this stage, trials could only be initiated by nose fixation. After a nose
poke of N¼1.5 s, either the Sþor the Sstimulus, chosen at random with
equal probability, was delivered to indicate the start of a trial. For S
trials, lever press responses in the T seconds (T¼6 s) following stimulus
delivery were unrewarded, and the audio prompt used in earlier stages
was never presented. For Sþ trials, the first lever press in the T seconds
(T ¼ 6 s) after the start of the trial was rewarded, as before. In Sþ trials
only, if no lever press response had occurred within P seconds after
stimulus delivery, an audio prompt was presented to the animal. This
delay P was increased from 0.125 s to T seconds and, as before, any
unfinished reward was removed after the trial’s end at T seconds. Thus,
responses to the audio prompt resulted in less time to drink than
responses that used the Sþ stimulus as a predictor. In both Sþ and S
trials, the stimulus was removed from the vibrissa field if nose poke
fixation was broken or the trial ended, whichever came first.
Acquisition of stimulus discrimination was indicated when the
number of lever press responses in the first P seconds of a trial
differed significantly between Sþ and S trials. The first P seconds
were used because an animal had access to additional information, in
the form of the cue, after P seconds. At this point, the audio prompt
was eliminated and performance was measured. For some animals, a
final parameter was varied during this testing stage. The number of
lever press responses L (Figure 7D) required to obtain a reward
increased from one to five, and the trial length T was increased to 8 s
to allow time for the longer behavioral response. This manipulation
increased the effort necessary to complete a full response in the go/
no-go task and discouraged the animal from responding if the
stimulus did not predict a reward. The direct use of air puffs as
negative reinforcement was unsuccessful at strengthening this
asymmetry of response, as it tended to lower the total number trials
rather than selectively suppressing S responses.
Fluid restriction and training sessions. Animals initially acclimated
to handling and to chocolate milk (Yoo-Hoo, Cadbury-Schweppes
[http://www.cadburyschweppes.com/EN]) from the fluid dispenser in
the behavioral chamber over a period of 2–3 wk. Animals were housed
in pairs and maintained on a standard light/dark cycle, and both
morning and evening training sessions were used. We did not observe
any significant effect of time of day or estrous cycle periodicity on
behavioral performance. Further, although chocolate milk was used
early in training, fluid-deprived animals appeared to perform equally
well for water rewards, which were preferred for ease of delivery.
for computer processing, solenoid switching, and the build-up of a
sufficient change in air pressure. The white-noise audio mask was
played continuously in the box to confound any auditory differences
between the stimuli.
Both carriage blocks and the bottom guide block (Figure S5B) were
drilled with matching hole patterns on a circle of 25-mm diameter
with either 15 8 or 7.5 8 spacing. The nose poke was bolted to the
bottom guide block and positioned such that a line connecting the
caudal edges of both mystacial pads would approximately coincide
with the center of this circle. A backstop was constructed by gluing 18gauge hypodermic tubing to the back of 90-mm lengths of the 0.86mm diameter stimulus rods. The backstops rested above the stimulus
carriage blocks and allowed the stimuli to travel with the carriage
blocks, extending from 10–61 mm below the floor of the bottom guide
block. This arrangement allowed the angular location of the stimuli to
be rapidly adjusted for each animal and was intrinsically safer for the
animals, as the stimuli dropped due to gravity rather than direct
piston drive. Our typical configuration fixed potential locations for
the stimuli at 3.758 þ n7.58 (where n is an integer between 5 and 5),
measured relative to a line through the center of the circle described
above and perpendicular to the animal’s midline. In all cases, one
stimulus was placed at a positive angle and another placed at a
negative angle; the angular difference and offset were adjusted for
each animal so that both rostral and caudal stimuli fell within the
range of vibrissa motion (Figure 6A, 6B, 6D, and 6E).
Video imaging. High-speed videography was used to characterize
the movement of the vibrissae once discrimination was established.
An IEEE-1394 monochrome complimentary metal oxide semiconductor camera (Basler Vision Technologies, 602f [http://www.
baslerweb.com]) with infrared sensitivity was mounted under the
elevated shelf in the training enclosure and focused on the plane of
the nose poke using a television lens (f/0.95, 17 mm, JML Optical
Industries, 71932 [http://www.jmloptical.com]) and a 45 8 mirror
under the stimuli (Figure 2A). Illumination was provided by an
infrared lamp (The LED Light, 850 nm peak [http://www.theledlight.
com]), which was modified to double output power, while strobed and
filtered at 850 nm to reduce leakage into the rat-visible spectrum. The
camera was interfaced to a personal computer running custom
LabVIEW software and typically acquired 360 3 300 pixel images at
200 Hz with a 1.2-ms exposure. Images were read into a circular
buffer, and 600 images were saved to disk 2.5 s after the start of each
behavioral trial, so that 0.5 s of pre-trial video was included in each
video sequence.
Video images were analyzed in MatLab (The Mathworks [http://
www.mathworks.com]). Gross head motion was extracted from the
videos to control for cases in which animals were able to break
fixation and reach the stimulus before it could be fully withdrawn.
Vibrissa motion was estimated from line-scan data extracted from an
image column over multiple time points (Figure 6B and 6E). The
median column over time was subtracted from each column to
remove stationary objects, and custom segmentation and tracking
algorithms (D. N. Hill and S.B. Mehta, unpublished) were applied to
estimate vibrissa position at each time point. This line-scan analysis
was performed on image columns ten pixels to the left and right of
the stimulus to avoid contamination from the motion of the stimulus
itself, and vibrissa position in the vicinity of the stimulus was
interpolated from a linear fit through these left and right position
estimates. Over these short regions, vibrissae were well approximated
with a linear fit; quadratic fits from three-point estimates showed
negligible contributions from the second-order coefficient. For
simplicity, line scans were used throughout rather than arcs, and
the position of the vibrissa tracks along the vibrissa length varied
slightly. In these tracks, the distance of the line-scan column from the
mystacial pad at 308 was approximately 15% greater than the distance
at 08. However, the placement of the stimuli was such that there was
no systematic difference in the length at which a vibrissa contacted
the rostral and caudal stimuli.
To identify potential contact events, the motion of the stimulus
was also extracted from the video (Figure S2). Epochs were identified
in which the vibrissa trajectory overlapped the stimulus position and
showed a velocity of no more than four pixels per frame (Figure 6H).
We used this heuristic because we lacked a bona fide detector for
stimulus contact and because image overlap of the vibrissa with the
stimulus did not necessarily correspond to physical contact in three
dimensions. However, this estimate of vibrissa contact was highly
accurate, as verified by manual inspection of the video corresponding
to a representative sample of contact events.
Operant shaping. The discrimination behavior was shaped in three
stages through classical operant training techniques (Figure 7) [70]. A
small number of parameters were varied in the behavioral program
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Figure S2. Duration of Stimulus Availability
(A) Overlaid stimulus motion traces from 58 Sþ and 56 S trials. A
stimulus descended after an animal had initiated a trial by placing its
nose in the nose poke and ascended when the animal first broke nose
poke fixation. The descent and ascent motions were estimated from
the video recordings and are plotted here. This motion was highly
repeatable and smooth; the descending traces appear jagged because
the stimuli traversed less than one camera pixel per frame. The
discretization evident in the stimulus ascent traces was due to the
finite sampling rate, i.e., 16 Hz, of the behavior computer.
(B) Distribution of stimulus availability times. The total time during
which the stimulus was in motion was determined from the traces in
(A) and is shown histogrammed here for Sþ and S trials. Note that
the animal moves out of the nose poke rapidly, i.e., 200–300 ms, in
most Sþ trials and waits longer in most S trials. This interval is
consistent with the time at which the lever press responses first
become distinct (Figure 4).
Found at doi:10.1371/journal.pbio.0050015.sg002 (716 KB EPS).
Upon reaching 230 g, animals entered a fluid restriction regimen
in which water was removed from their home cage 16–23 h before
training to increase motivation. Animals were allowed ad libitum
fluid access two days a week, and weights were monitored daily. We
used a variable restriction schedule for two reasons. First, the total
duration of the training ranged from 6–12 mo, and the long-term
health of the animals was a concern. Second, increased pretraining
fluid deprivation did not correlate strongly with an increased number
of trials per session. Further, the longest deprivation durations we
tried, i.e., 24 h, at times caused animals to respond indiscriminately to
both Sþ and S stimuli. Restriction duration was thus tuned
separately for each animal.
Daily training sessions were 20–30 min in duration. The physical
proximity of the tactile stimulus and response apparatus allowed
animals to perform a large number of trials in this amount of time; a
total of 50 trials was typical in intermediate stages of training, and a
total of 100 trials, of which approximately 50 were rewarded, was
typical of well-trained animals on the full discrimination task. These
large numbers of trials were needed to obtain statistical evidence of
discrimination, and we thus required animals to perform at high
rates. As such, five of the initial cohort of 24 rats were removed early
in training, i.e., after fewer than 30 sessions, because they performed
significantly fewer trials than their littermates. A further five animals
were removed at intermediate stages, i.e., after approximately 100
sessions, for performing small numbers of trials after the lever and
nose poke were introduced. We did not consider these ten animals in
the summary analysis shown in Figure 3, because they were not
introduced to the stimulus.
For the remaining 14 animals, the number of sessions required to
acquire the lever press response and nose fixation of 1.5 s ranged
from 225 for our earliest animals to 61 for animals who started
training later in the study. This large reduction in the number of
sessions occurred as the training procedures described above were
established, and the earlier numbers reflect our adjustments to these
procedures rather than the intrinsic time needed to train these
behaviors. Further, we chose relatively short session durations to
facilitate the concurrent training of multiple animals as we developed
the procedures described above. In many cases, however, animals
would still be performing trials at the end of a session, albeit at a
decreasing pace. It is thus likely that the use of our eventual protocol
with longer sessions to obtain more trials per animal per day would
have further decreased the training time necessary to achieve this
level of behavioral performance.
The number of sessions required to learn the stimulus task was
more variable, ranging from 17 to 75, and did not reliably decrease
over the course of the study. Further, this measure did not appear
correlated with eventual performance as the vibrissae were trimmed.
Vibrissa trimming. Animals that successfully discriminated their
assigned Sþ and S stimuli in the absence of the audio prompt (Figure
7D) in multiple consecutive sessions were then trained with only a
single vibrissae row intact. At least once per week, animals at this
stage were lightly anesthetized on isoflurane for vibrissa trimming. All
vibrissae on the left side and all vibrissae on the right side except for
the C row were cut. Animals continued training with a single row
until they again demonstrated successful discrimination in multiple
consecutive sessions, at which point their vibrissae were further
trimmed to leave only a single vibrissa intact. This vibrissa was
required to be sufficiently long to reach the stimuli and was thus
typically chosen to be C1. Animals that performed successfully with a
single intact vibrissa were recorded on video as described above and
finally challenged with a series of controls.
Figure S3. Evolution of Lever Press Response Distribution
The mean cumulative lever press count as a function of time (Figure
4B) does not convey information about the distribution of responses.
For example, a mean count of 0.5 responses at 1.0 s could arise from
equal numbers of trials with zero responses and with one response, or
it could come from many zero response trials and a few trials with two
or more responses. Because we relied on the separation of these mean
cumulative curves to establish the time scale of the perceptual
computation, we show here the complete response distributions
corresponding to the mean curves.
(A) Response distributions for 58 Sþ trials. At each point in time, the
distribution of cumulative lever press counts is plotted such that each
column in the image sums to 1.0. The weighted average of each
column is equivalent to the mean cumulative response (Figure 4B).
The top row shows the fraction of trials that have reached five lever
presses as a function of time (equivalent to the cumulative
distributions in Figure 4C).
(B) Response distributions for 56 S trials. Note that a fraction of the
trials never reach five lever press responses. Our conclusion that the
Sþ and S responses diverge after 250 ms (gray arrows in Figure 4B) is
reflected here by the overall rightward shift, at all cumulative counts,
for the data shown in (B) relative to those shown in (A).
Found at doi:10.1371/journal.pbio.0050015.sg003 (812 KB EPS).
Figure S4. Complete Stimulus Assembly, Including Support Structures Omitted from Figure 2
The rostral stimulus is shown in a position that would overlap with
the vibrissa field, and the caudal stimulus is shown fully retracted.
(A) Three-dimensional perspective. The large horizontal rectangular
block is the main platform. Two air-driven pistons are held above this
block. Each of these pistons independently drives a carriage that
supports a stimulus pin. A hole pattern in the carriages matches the
guide pattern inset into the stimulus platform, and these patterns
together define repeatable stimulus positions. The Teflon rods on
which the carriages travel are shown in brown. The nose poke is the
cylindrical black object hanging below the main platform, and it
defines the position of the rat relative to the stimulus hole patterns.
(B) Front view.
(C) Side view.
Found at doi:10.1371/journal.pbio.0050015.sg004 (848 KB EPS).
Figure S5. Detailed Schematics of Stimulus Assembly Main Platform
and Guide
(A) Main platform. This Lexan platform rested above the rat (as
described in Methods and Figure 2) and supported the stimulus
assembly.
(B) Stimulus guide. This Lexan block was inset into the main platform
and provided guide holes to direct the stimulus pins to various angles
on a 25-mm radius. The nose poke was positioned under the main
platform such that a line connecting the caudal edges of both
mystacial pads would coincide with the center of this circle.
Found at doi:10.1371/journal.pbio.0050015.sg005 (795 KB EPS).
Supporting Information
Figure S1. Stimulus Position Relative to the Full Vibrissa Field
Video still images of rats in the stimulus assembly nose poke (see also
Figure 6B and 6E). (A), (B), and (C) each show both side and bottom
views. The two views in each panel were not taken simultaneously but
show comparable times in a behavioral trial. The scale bar in all cases
is 4 mm.
(A) Rat with all vibrissae intact. Note the large span of the vibrissa
field in both rostrocaudal and dorsoventral directions.
(B) Rat with only C row intact. The C3 vibrissa is shown contacting the
rostral stimulus. The green arrows point to the location of contact.
(C) Rat with only the C row intact. The c stradler is shown contacting
the caudal stimulus. The red arrows point to the location of contact.
This stimulus is 308 caudal to the stimulus shown in (B).
Found at doi:10.1371/journal.pbio.0050015.sg001 (4.5 MB EPS).
PLoS Biology | www.plosbiology.org
Figure S6. Detailed Schematics of Stimulus Assembly Piston Support
and Carriage
(A) Piston support bracket. This fixed Lexan block held the body of
the air pistons in place. Precision Teflon rods connecting the bracket
to the main platform ensured that piston travel was perpendicular to
the stimulus guide.
0012
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Active Touch Perception
We thank O. Kuti and L. Pockros for technical assistance and E.
Ahissar, J. C. Curtis, M. S. Fee, D. N. Hill, P.M. Knutsen, E. R. Macagno,
and J. B. Wolfe for discussions related to this work.
Author contributions. SBM, DW, and DK conceived and designed
the experiments. SBM, DW, and RF performed the experiments. SBM
analyzed the data. SBM, BAW, and DK contributed reagents/
materials/analysis tools. SBM and DK wrote the paper.
Funding. Supported by the Human Frontiers for Scientific
Progress (RGP43/2004 to DK), United States–Israeli Binational
Science Foundation (2003222 to DK), National Science Foundation
Integrative Graduate Education and Research Traineeship program
(to DW), and the Howard Hughes Medical Institute predoctoral
fellowship program (to SBM).
Competing interests. The authors have declared that no competing
interests exist.
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